The PRI Apple Breeding Program Jules Janick Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, in 47907-1165

The PRI Apple Breeding Program Jules Janick Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907-1165

ORIGINS and initiated an intensive study of crosses been under investigation. (In the l940s, consider- between cultivated apples and crab-like forms. able interest in the genetics of the ascomycetes The PRI cooperative scab-resistant apple A summary of Crandall’s work, published in had been engendered by the work of Beadle and breeding program between Purdue University, University of Illinois Bulletin 275 (Crandall, Tatum in Neurospora.) Shay and Hough decided Rutgers, The State University of New Jersey, 1926), describes all the material in the program. to collaborate on a scab-resistance breeding and the University of Illinois has a long and Crandall, infl uenced by the rediscovery of Men- program with the objective to advance genetic interesting history involving many scientists del, was attempting to determine inheritance resistance identifi ed by Hough into improved and collaborators (D.F. Dayton, “A history of patterns in Malus. Ironically, he did not work horticultural backgrounds and identifi cation of the Illinois–Indiana–New Jersey cooperative with characteristics that would enable him to additional resistant Malus germplasm through apple breeding program,” unpublished; Crosby identify single genes or evaluate his material testing of material in arboreta and other collec- et al., 1992; Janick, 2002). The original program for disease resistance. The voluminous data he tions. The fi rst screened hybrid progenies were dates to a formal 1945 collaboration between J. collected and maintained at the University of planted in the fi eld in 1947 and began fruiting at Ralph Shay (1918–1980), pathologist at Purdue Illinois has never been completely analyzed, Illinois in l951. A formal cooperative program University, and L. Fredric Hough (1915–1993), although the designations reported in Bulletin was established in 1945 between the agricultural horticulturist at the University of Illinois, to 275 describing his species sources have become experiment stations associated with Purdue develop scab-resistant apples. Shay was a justly famous. The selection he labeled Malus University and the University of Illinois. man of vision who was enthusiastic about his fl oribunda 821 was the original source of the

work and about science in general. He had an Vf gene. Fortunately, his breeding material was THE TEAM outgoing personality, made friends easily, and maintained following his retirement in 1927, but had the ability to stimulate enthusiasm in others. remained unevaluated until L.F. Hough joined In 1948, Hough moved to the Department Hough was an extraordinary fruit breeder, full of the department in 1942 as a graduate student of Horticulture and Forestry at Rutgers, The optimism, whose credo of “one more genera- and plant-breeding assistant. State University of New Jersey, and, shortly tion” typifi ed his philosophy of fruit breeding, Spring 1943 was unusually cool and wet, thereafter, Rutgers joined Illinois and Purdue which was to cherish diversity, pollinate with resulting in a severe epidemic of scab that de- as the third partner in the collaboration, thereby abandon, and extravagantly share seedlings with foliated all susceptible unsprayed apples trees. making available to the program a large volume

everyone. Pollination was his happiest time as Hough noted that one progeny, an F2 of M. of valuable susceptible apple germplasm devel- he, with carloads of students, pursued Spring fl oribunda 821 × Rome Beauty, segregated at oped by the late M.A. Blake. In 1950, Daniel in her northward trek in an attempt to improve a ratio of 1 resistant : 1 susceptible, suggesting F. Dayton joined the program at Illinois while

the odds for favorable recombinants—always the involvement of a single gene, later termed Vf. pursuing graduate studies. Dan was a witty, just a generation away. Interestingly, the PRI Hough published his results with the Proceed- energetic New Englander from New Hampshire program was initiated before the environmental ings of the American Society of Horticultural who was equally at home in the orchard as implications of pesticides were realized, and Science in his famous paper “A Survey of the improvising on the organ. Edwin B. Williams, the goal was simply one of serving the needs Scab Resistance of the Foliage of Seedlings a graduate student of Shay’s in plant pathology, of fruit growers. in Selected Apple Progenies” (Hough, 1944). a native Hoosier, and a World War II veteran The germplasm exploited by Shay and The paper was brought to the attention of J.R. who had served in the Philippines, became a Hough can be traced to breeding studies of Shay, a young professor who joined the Purdue’s skilled pomologist to complement his abilities C.S. Crandall (1852–1929) at the University Department of Botany and Plant Pathology from as a pathologist, fi sherman, and poker player. of Illinois carried out as early as l907. Crandall Arkansas and who had received his PhD from Dayton and Williams remained with the program had assembled a large collection of Malus spe- the University of Wisconsin where a program upon completion of their PhD degrees (Fig. 1). cies and forms at the beginning of the century on the pathogenicity of Venturia inaequalis had Dayton continued leadership for the Illinois

Fig. 1. Dan Dayton, Jules Janick, Ed Williams, Fred Hough, and Ralph Shay (left to right).

8 HORTSCIENCE VOL. 41(1) FEBRUARY 2006

FFebruaryBookebruaryBook 1 8 112/14/052/14/05 110:47:480:47:48 AAMM Table 1. Defi ned gene pools for resistance to apple races of the fungus. Progeny segregation ratios England under the assistance of the late A.G. scab. and the frequency distribution of leaf reaction Brown of the John Innes Institute. Symbol Original Malus source classes suggest the complexity of the genetic The original breeding program was basis of resistance derived from V . uniquely a true cooperative effort between Vf M. fl oribunda f Vm M. micromalus (pit) The goals of the program were 2-fold: the three stations. While crossing was carried Vr M. pumila (Russian) 12740-7A genetic improvement of apple and an eluci- out at each location, the bulk of the successful (probably M. seversia) dation of the genetics of resistance in apple. hybridizations were achieved by Hough, who V M. baccata jackii bj The breeding strategy consisted of a modifi ed each spring traveled with his team of pollinators V Hansens’s baccata #2 b backcross program with the entire spectrum from New Brunswick, N.J., to Geneva, N.Y., V Antonovka PI 1722623 (pit) a of susceptible cultivars serving as recurrent and on to New Hampshire, following spring parents. Several Malus species were used in its northern trek. All seeds were assembled team, with Williams assuming leadership of to incorporate their resistance factors into at Purdue University and screened for scab at the Purdue program when Shay left to join the more advanced pomological backgrounds. the Department of Botany and Plant Pathol- University of Oregon in 1966. J.B. Mowry, sta- The extensive effort to evaluate the nature of ogy. Resistant seedlings were either planted tioned at the Illinois Horticultural Experiment resistance and the stability of resistance was directly to the fi eld or grown in a nursery and Station, Carbondale, joined the collaboration carried out in studies parallel to the breeding then divided between cooperators, with the in 1952 and tested material until his death in program. Many Malus species and hybrids bulk of the progenies evaluated in Indiana 1986. In 1955, Catherine H. Bailey, a gradu- with genetic resistance useful in breeding were and Illinois. Fruit of promising seedlings each ate student of Hough and research associate, subsequently identifi ed. Through a series of year were compared in a joint display and used became a participant at Rutgers. I joined the intercrosses (tests of allelism) it was established in crosses in the following years. By 1967 Purdue program in 1954 and, by a curious set that 11 of the 25 sources were due to the same the most promising selections, called co-ops of circumstances, became the last man stand- Vf gene (Williams and Kuc 1969). Six loci for to underscore the cooperative nature of the ing of the original PRI group (Fig. 1). Frank qualitative resistance (defi ned gene pools) were program, were released to interested testers H. Emerson was a part of the program from identifi ed as shown in Table 1. including fruit growers and experiment stations 1967 to 1988. Schuyler S. Korban replaced Five different virulent races of V. inae- in other states. In addition, promising selec- Dayton at the University of Illinois upon his qualis were identifi ed, and race 6 has been tions were shared worldwide with international retirement in 1982. Shawn A. Mehlenbacher subsequently identifi ed in Germany (Parisi et cooperators. replaced Hough after his retirement in 1981, al., 1993) as shown in Table 2. Recently, race remained with the program from 1982–1986, 7 has appeared and attacks M. fl oribunda 821 ACCOMPLISHMENTS and was in turn replaced by Joseph Goffreda in and questions the durability of the Vf gene 1989. Other participants in PRI included Jeffry without modifi ers. Fortunately race 7 does Up to the present time, more than 1500 A. Crosby and Paul C. Pecknold at Purdue not attack ‘Golden Delicious’, which indicates selections have been made of which 44 have University, P.A. O’Connor and S.M. Ries at the the presence of modifi ers in this cultivar (Y. been released for advanced testing as co- University of Illinois, and A. Voordeckers at Lespinasse, personal communication). ops, and, of these, 16 have been named as Rutgers University. H.F. Goonewardene, a U.S. In addition to screening for apple scab, shown in Table 3. Joint releases from other Department of Agriculture employee stationed screening for other diseases was carried out in PRI selections include ‘McShay’ (1988), at Purdue, investigated insect resistance in PRI the fi eld from natural infection. These included released in cooperation with Oregon State germplasm from 1973 to 1988. fi reblight incited by Erwinia amylovora (Burr. University;‘Priam’(1974) and ‘Juliet’ (1999), A) Winslow et al., cedar–apple rust incited released in France; ‘Primiera’ (1995), released TECHNIQUES AND STRATEGY by Gymnosporangium juniperi-virginianae in Italy; ‘Primivera’ (1996), released in Que- Schw., and powdery mildew incited by Po- bec, Canada; and ‘Constance’ (1995), released Techniques for controlled greenhouse dosphaera leucotricha (Ell. & Ev.) Salm. in Germany by an organic grower. ‘Nambu’ screening of hybrid progenies were developed Some screening for mildew was carried out in (1994) is a PRI selection that was released by Shay, thus making it possible to identify resistant segregates within 2 months after Table 2. Races of Venturia inaequalis and differential hosts of apple. seed germination. Resistance of apple to scab Race Source Susceptible material was scored according to symptoms on young 1 Worldwide Most of the world’s cultivars leaves grown under greenhouse conditions: 2 South Dakota M. baccata, ‘Dolgo’, ‘Alexis’, ‘Bittercrab’ segregates of 0 = no macroscopic evidence of infection; 1 R12740-7A, ‘Geneva’ = pinpoint pits, no sporulation; 2 = irregular 3 Nova Scotia, Canada ‘Geneva’ chlorotic or necrotic lesions and no sporulation; 4 Lafayette, Ind. Segregates of R12740-7A 3 = few restricted sporulating lesions; and 4 = 5 Norwich, England Micromalus pit type resistance, M. atrosanguinea 804 extensive, abundantly sporulating lesions. The 6 Ahrensburg, Germany ‘Prima’ (Vf cultivars) but not ‘Evereste’ M. × ‘Perpetu’ class M was added to indicate a mixture of and M. fl oribunda 821 7 England–Europe M. fl oribunda 821 necrotic, nonsporulating, and sparsely sporu- lating lesions (Shay and Hough, 1952). Only Table 3. PRI and joint releases of scab-resistant apples. class 4 was considered as fi eld-susceptible; all the others classifi ed as fi eld-resistant and PRI releases Co-op no. Year released Joint releases Co-op no. Year released did not show symptoms of infection when Prima 2 1970 Priam --- 1974 grown outdoors where conditions for scab are Priscilla 4 1972 McShay --- 1988 very favorable. Using a broad defi nition of Sir Prize 5 1975 Primiera 42 1995 Jonafree 22 1979 Nambu --- 1994 resistance, crosses of heterozygous-resistant Redfree 13 1981 Constance --- 1995 with homozygous-susceptibles segregate 1 Dayton 21 1988 Primivera --- 1996 resistant : 1 susceptible but usable resistance Williams’ Pride 23 1988 Juliet 43 1999 (completely nonsporulating, i.e., class 0, 1, Enterprise 30 1993 and 2) is lower, typically 30%. For example, GoldRush 38 1993 Pristine 32 1994 although Vf is traditionally considered to be a simply inherited, dominant factor conditioning Scarlett O’Hara 25 2000 qualitative resistance, it is often associated with Pixie Crunch 33 2004

any number of quantitative resistance factors Sundance 29 2004 CrimsonCrisp 30 2005 that make it less vulnerable to attack by new

HORTSCIENCE VOL. 41(1) FEBRUARY 2006 9

FFebruaryBookebruaryBook 1 9 112/14/052/14/05 110:47:540:47:54 AAMM without authorization in Japan. ‘Viking’ FUTURE PROSPECTS CONCLUSIONS (1969), released in Wisconsin, is a PRI selec- tion but proved to be scab-susceptible. The excellent progress in developing new The PRI program remains as an example of An attempt was made to carry each source apple scab-immune cultivars was due to ad- what can be accomplished in tree-fruit-breed- of resistance forward, but resistance derived ministrative support at the three institutions, ing programs, long discounted for their slow from M. fl oribunda received the most attention the ability and willingness of the cooperating progress, by a concerted attempt at transferring workers to pool their efforts and facilities, because two F2 selections of the original M. desirable genes from interspecifi c hybridiza- fl oribunda 821 × Rome Beauty cross carrying and the tremendous effort carried out in the tion. Several serendipitous discoveries were Purdue University Department of Botany the designation F2 26829 and F2 28830 were made. By impatiently using the fi rst fruiting more advanced in size and quality. Selection and Plant Pathology, under the guidance fi rst selections from crosses as parents, reduced ju- of J.R. Shay and later of E.B. Williams, to F2 26829, while only two generations from the venility and increased precocity were selected. original small-fruited species, had unusually carry out an effi cient greenhouse screening The advantages of diversity were demonstrated good quality and was about 5 cm in diameter. procedure. About 380,000 seedlings were by the incorporation of a tolerance to a number A breakdown of the pedigrees of the 44 co-op screened. Although the scab-resistance pro- of insects and diseases and long storage abil- selections indicates that all of the 44 released gram still exists between the three institutions, ity. The impact of the program is expected to date back to M. fl oribunda, although Co-op 41 activity has declined as the universities at be fully realized in the 21st century, as more also has M. atrosanguinea 804 in its pedigree. each location reduced support. By 1993 the breeding programs worldwide incorporate Of the 43 fl oribunda selections, only one co- Department of Botany and Plant Pathology this disease resistant material developed by op derived from 26830 entirely (Co-op 11), discontinued its input and I carried on the the PRI program. Purdue program, being directed to be con- one has both F2 26829 and F2 26830 in its cerned only with evaluating the remaining Literature Cited and Further Reading pedigree, and three have F2 26829 on both sides. The scab-resistance program at Cornell selections, although crossing continued. At the University of Illinois, Korban’s program Crandall, C.S. 1926. Apple breeding at the University University originated from material derived of Illinois. Univ. Ill. (Urbana) Agr. Expt. Sta. from F 26829 and the two releases ‘Liberty’ became oriented to the molecular biology of Bul. 275. 2 scab resistance. Screening has continued at and ‘Freedom’ carry the Vf gene. Crosby, J.A., J. Janick, P.C. Pecknold, S.S. Korban, P.A. In 1963, the three cooperating universi- Rutgers, but the apple-breeding program is O’Conner, S.M. Ries, J. Goffreda, and A. Voordeck- ties, in conjunction with other interested just one small part of a general fruit-breeding ers. 1992. Breeding apples for scab resistance: American and Canadian breeders, formed program. However, just as the universities 1945–1990. Fruit Var. J. 46:145–166. a loose cooperative organization known as were fatigued with funding, a number of Hough, L.F. 1944. A survey of the scab resistance of The Apple Breeder Cooperative (ABC), and fruit growers became believers in the pro- the foliage on seedlings in selected apple progenies. Proc. Amer. Soc. Hort. Sci. 4:260–272. workers in several other states have partici- gram and formed an organization called the Midwest Apple Improvement Association to Janick, J. 2002. History of the PRI apple breeding pated in testing selections. Introductions of program. Acta Hort. 595:55–59. the co-op selections and the release of scab- continue the breeding efforts. Crosses have Janick, J., J.H. Cummins, S.K. Brown, and M. Hemmat. immune cultivars created great interest in been made at Purdue and are supplied to the 1996. Apples, p. 1–77. In: J. Janick and J.N. Moore the program throughout the world. Several organization. Screenings in l998, 1999, and (eds.). Fruit breeding. Wiley, New York. countries, including Australia, Brazil, Canada, 2000 were carried out by Diane Doud Miller Parisi, L., Y. Lespinasse, J. Guillaumes, and J. Küger. Czechoslovakia, England, France, Italy, Po- at Ohio State University. At the same time, 1993. A new race of Venturia inaequalis virulent land, South Africa, Romania, Sweden, and international interest in scab resistant breeding to apples with resistance due to the Vf gene. Phy- Russia, have incorporated PRI germplasm has continued in Europe. topathology 83:533–537. PRI (Purdue Univ., Rutgers Univ., Univ. Illinois) in their apple-breeding programs. By 2000, disease resistant apple breeding program. www. more than 50 scab resistant selections had hort.purdue.edu/newcrop/pri. been released. Shay, J.R. and L.F. Hough. 1952. Evaluation of apple scab resistance in selections in Malus. Amer. J. Bot. 39:288-297. Williams, E.B. and J. Kuc. 1969. Resistance in Malus to Venturia inaequalis. Annu. Rev. Phytopathol. 7:223–246.

10 HORTSCIENCE VOL. 41(1) FEBRUARY 2006

FFebruaryBookebruaryBook 1 1100 112/14/052/14/05 110:47:570:47:57 AAMM